Primate Anatomy: An Introduction

Primate Anatomy

An Introduction

Third Edition

Friderun Ankel-Simons

Department of Biological Anthropology and Anatomy Duke University Durham, North Carolina

Academic Press

Table of Contents

Cover image

Title page

Foreword to the Second Edition

Preface

Preface to the First Edition

Chapter 1: Taxonomic List of Extant Primates

Publisher Summary

NEW DEVELOPMENTS

LIST OF EXTANT PRIMATES

Chapter 2: Taxonomy

Publisher Summary

HIERARCHICAL CLASSIFICATION

POPULATION BIOLOGY AND CLASSIFICATION

MISUNDERSTANDINGS IN PRIMATE CLASSIFICATION

THE TARSIER CONUNDRUM

Chapter 3: A History and Objectives of Primatology

Publisher Summary

THE STATE OF AFFAIRS

HISTORY

PRIMATOLOGY AS A BRANCH OF BIOLOGY

THE FUTURE OF PRIMATOLOGY

RETROSPECTION AND PREDICTION

DEFINITION OF ORDER PRIMATES

Chapter 4: Survey of Living Primates

Publisher Summary

SURVEY OF LIVING SCANDENTIA AND PROSIMII

SURVEY OF LIVING ANTHROPOIDEA

Chapter 5: Skull

Publisher Summary

SKULL DEVELOPMENT AND THE TWO TYPES OF BONE

ORBITAL REGION

NASAL REGION

SKULL BASE, BRAINCASE, AND FORAMEN MAGNUM POSITION

EAR REGION

THE SINUSES

COMPARATIVE PRIMATE SKULL MORPHOLOGY

Chapter 6: Brain

Publisher Summary

BRAIN MORPHOLOGY

GENE EXPRESSION

NEW INSIGHTS INTO BRAIN FUNCTION

Chapter 7: Teeth

Publisher Summary

TOOTH MORPHOLOGY AND DIET—CAN THEY BE RELIABLY CORRELATED?

TOOTH STRUCTURE

DENTAL FORMULAE

DENTAL TYPOLOGY

FUNCTIONAL AND MORPHOLOGICAL VARIATION

DENTAL FORMULAE AND MORPHOLOGY

WHAT IS NEW IN PRIMATE TOOTH RESEARCH?

Chapter 8: Postcranial Skeleton

Publisher Summary

SPINE AND THORAX

SHOULDER GIRDLE

PELVIC GIRDLE

HANDS AND FEET

FIFTH EXTREMITY

MUSCLES

LOCOMOTION

NEW TECHNOLOGIES APPLIED TO STUDY PRIMATE LOCOMOTION

Chapter 9: Sense Organs and Viscera

Publisher Summary

NOSE AND OLFACTION

ORAL CAVITY, TONGUE, AND TASTE

AUDITORY REGION, HEARING, AND VOCALIZATION

EYES AND EYESIGHT

PRIMATE DIARHYTHMS AND BIOCHRONOLOGY

NUTRITION AND THE INTESTINAL TRACT

TOUCH

Chapter 10: Placentation and Early Primate Development

Publisher Summary

LEMURIDAE AND LORISIDAE

TARSIIDAE

CEBOIDEA AND CERCOPITHECOIDEA

CALLITRICHIDAE

PONGIDAE AND HOMINIDAE

Chapter 11: Reproductive Organs, Reproduction, and Growth

Publisher Summary

Chapter 12: Chromosomes and Blood Groups

Publisher Summary

CHROMOSOMES

BLOOD GROUPS

Chapter 13: Molecular Primatology

Publisher Summary

THE GENETIC MATERIAL OF CELLS

INDIRECT METHODS TO STUDY MOLECULAR PRIMATOLOGY

DIRECT STUDY OF GENETIC MATERIAL

PROBLEMS OF PHYLOGENETIC ANALYSIS USING MOLECULAR DATA

Chapter 14: Primate Genomics

Publisher Summary

THE HISTORY OF GENETICS

MOLECULAR PHYLOGENETICS

THE TARSIER CONUNDRUM STILL NOT SOLVED

GENETIC EXPRESSION OF HUMAN LEARNING

BAC, YAC, AND PAC LIBRARIES

GENES CONTROLLING HUMAN BEHAVIOR

VIEW INTO THE FUTURE OF GENOMICS

TRANSPOSABLE ELEMENTS AND NUMTS

OUTLOOK AND REFLECTION

Chapter 15: Conclusions with a Glance at the Future

Publisher Summary

Bibliography

Index

Foreword to the Second Edition

It is a pleasure and an honor to be asked to write the foreword to the second edition of Primate Anatomy: An Introduction by Friderun Ankel-Simons, a dear friend for nearly thirty years.

Anyone attempting to survey the comparative anatomy of primates has my highest respect for a task that can only be described as daunting, if not impossible. Since introductory books on the anatomy of the best known species, Homo sapiens, fill hundreds of pages a volume, the goal of covering all 250 or so living species in a few hundred pages requires tremendous research in an arcane literature written in many languages and then draconian summarization. However, any attempt at balance is further undermined by the fact that the anatomy of many species is virtually unknown and for others the coverage is very uneven. We can only hope that many of these poorly known species can be studied before they become extinct.

Yet these gaps in the primary literature only emphasize the need for a general book on this subject. Students of both living and fossil primates, indeed anyone interested in understanding ourselves, in our biological context, need a book that summarizes what is known of primate anatomy in a readily accessible form. The longtime classic, Le Gros Clark’s 1963 Antecedents of Man, has long been out of print and Dr. Ankel-Simons’s first edition is nineteen years old now.

Other attempts to cover this material such as the largely unavailable Primatologia, Handbook of Primatology, are far too specialized for student readers, as are the many edited books and papers on specialized topics.

In writing this book, Dr. Ankel-Simons brings an impressive set of credentials and diverse experiences. Originally trained as a marine biologist, she has the biologist’s ability to see humans and other primates in the context of the whole animal kingdom. However, she subsequently received her primatological training at the Anthropological Institute of Zürich, Switzerland, under the tutelage of the great Adolph Schultz, who contributed more to our knowledge of primate skeletal anatomy than anyone before or since. She taught primatology for seven years at the institute of anthropology in Zürich, and in recent decades has held positions at Yale University, Brown University, Duke University, and the Duke Primate Center, and gained considerable knowledge about both living and fossil primates through research in Egypt and Madagascar.

In this new edition, Dr. Ankel-Simons has brought all of her experience to bear and produced a worthy successor to her first edition and a book that will be valued by students and professionals for many years.

John G. Fleagle,     Department of Anatomical Sciences, State University of New York at Stony Brook

Preface

Whatever my hearers might do, I myself always learned sometimes by lecturing. And to those who have experience of what a heart-breaking business teaching is—how much the can’t-learns and won’t-learns and don’t-learns predominate over the do-learns—(sic) will understand the comfort of that reflection.

Thomas Henry Huxley (1896)

We humans are classified together with our closest relatives among living things: Lemurs, lorises, galagos and tarsiers, monkeys of the New and Old Worlds, lesser apes or gibbons, greater apes, and humans are all members of the mammal order Primates. The biological science studying humans together with their mammalian relatives is called primatology.

Primatology really only exists because mankind has a unique place within the order Primates. No human would pay any more attention to this order of mammals than to any other group of living creatures were it not for our unique interest in understanding our own place in biological nature.

It has been a long time since biologists drew their phylogenetic trees by hand and the results looked like the real thing. Ernst Haeckel’s tree (1874) is a beautiful example (Figure 1). Today such trees—now also known as cladograms—are constructed by computers and look like stick figures. They are far removed from reality.

Figure 1 An ancient amazing tree, depicting human phylogeny at the time, hand drawn by Ernst Haeckel, 1874.

Figure 2 The aye-aye (Daubentonia madagascariensis), the most remarkable of primates, from the 1863 monograph by Sir Richard Owen.

Whether we have made much progress since real trees depicted phylogenetic concepts is an important question that we should never forget to keep asking ourselves. Somehow it seems important that we keep in mind that phylogenetic trees used to be real, not abstract. Today, primatology should endeavor to stay close to the biological nature of all primates, humans included. Cladistic stick trees are unnatural for various reasons. Biochemical particles such as DNA molecules are infinitely tiny and not alive when they are studied. These modern entities are far removed from the reality and the magic of real life, the magic of real trees, and the magical beauty of the diademed Sifaka, whose likeness is on the cover of this volume. So let us not neglect nature’s reality. Let us always remember that we are biologists who are studying living things and that we should have respect for nature.

In the following chapters I shall attempt to guide the reader through the basics of knowledge that any student of our closest relatives, the primates, must grasp to become a primatologist.

The book opens with a taxonomic list of extant primates. The list presented here does not and cannot represent absolute truth as carved in stone. Taxonomic concepts are constantly in flux, partly because new species, even new primates, are being discovered and newly described. Often new insights into relationships between genera and species can change taxonomic assignments (e.g., the placement of the enigmatic South American monkey genus Callimico with either callithrichids or cebids). Nevertheless, it is important that discussions of extant primate groups be placed into a clear framework of relationships and names to prevent confusion. Taxonomic changes should be introduced only when they have become properly established and are obviously reasonable: Scientific dialogues are useful only when they use the same terminology. In 2001 the excellent volume on primate taxonomy by Colin Groves was published and has become the fundamental source for any discussion about primate relationships. But since then many changes of assignments have been suggested. Taxonomy continues to be a lively topic. There has been much rearranging of systematic assignments and naming of new taxa since January 2000, when the second edition of Primate Anatomy: An Introduction was published.

Chapter 2 introduces the reader to perpetual complications of taxonomic procedures, explaining the puzzling, but widely used, cladistic terminology (as it originated from the work of Willi Hennig (1966).

In Chapter 3 the reader will find an outline of the history and objectives of primatology. A definition of the order Primates is undertaken. Chapter 4 surveys the living primates, briefly describing and characterizing the biology and distinguishing characters of each primate genus. In Chapter 5 the anatomical details of the skull are reviewed, and Chapter 6 takes up the morphological and developmental characteristics of the brain. Chapter 7 presents the developmental and functional morphology of teeth. The postcranial skeleton together with the role of musculature and the variation of primate locomotion are detailed in Chapter 8.

Chapter 9 deals with the senses and their genetics: nose and olfaction, the oral cavity, the tongue, and the function of taste. Since the last edition of Primate Anatomy: An Introduction was published, great inroads have been made in understanding of function and importance of olfactory signals (Wyatt, 2003). Also, the auditory region and hearing as well as eye and eyesight are profiled in this chapter. Particularly the new understanding about function and perfection of vision among primates and their genetic manifestation have had great bearing on the need to totally revise the section on vision. Here I would like to especially thank Pat Wright, Patrick O’Connor, Tab Rasmussen, and James Pettigrew for many helpful interactions. Later in this chapter, diarhythms and biochronology are discussed. Next, the importance of diet and nutrition and the function and differences of the primate intestinal tract are the focus. The sense and sensibility of touch conclude Chapter 9.

In Chapter 10 the nature and role of placentation and early development in primates are presented. Placentation, reproductive organs, reproduction, growth, and development are detailed in Chapter 11. Chapter 12 deals with chromosomes and blood groups of primates, and Chapter 13 again offers a survey of new developments in molecular primatology, molecular clocks, the role of mitochondrial DNA, and problems of attempting to understand phylogeny using molecular data. Chapter 14 represents one of the first endeavors to summarize the vast new world of primate genomics. A short concluding chapter provides the reader with an overview of the state of primatology and humanity today and peers into their precarious future. A bibliography and an index of important terms conclude the volume.

I shall now tell the story of Primate Anatomy: An Introduction and how it came about. It is a tale with some intriguing and totally unpredictable convolutions and detours.

After I had taught all about primates for more than seven years at the University of Zürich, I decided to compile and consolidate as much primatological information as possible and to make it easily accessible. The result was the first German language Introduction to Primatology (Ankel, 1970). Then and now much of what I have learned and know about primates came from the never-ending and enjoyable dialogue with my students, first in Europe, and later in the United States. This exchange still continues. Even today much crucial information about living primates remains scattered randomly in professional journals and specialized books. Access is therefore often too burdensome and costly for teachers and students alike. Even though much information is now available on the Internet, scientific volumes and journals have become forbiddingly expensive. When I started to assemble the information that I had gathered over years of teaching, no survey of living primates was available in German. A year after publication of the small volume Einführung in die Primatenkunde, I came to the United States and was asked if my German Introduction to Primatology might be translated into English. There was no English textbook like it dealing with the basics of primatology. After lengthy negotiations about a possible translation, it became evident that a new and more detailed and up-to-date book would be the better solution. After signing a contract with the College Division of Macmillan Publishers in New York, I set to work. The textbook was scheduled to be published in the Macmillan Series in Physical Anthropology. Soon, however, the progress of this endeavor was slowed by such important events as marriage and the births of two children. Inasmuch as I am convinced that infant human primates need the devoted and undistracted attention of a mother, time to write a book about primates took a backseat to providing a solid and functional family life for a while. Yet finally the first edition of the book that, by necessity, was produced in an on-and-off fashion was published in 1983. However, an unanticipated and bizarre development caused the book’s premature demise.

The Macmillan press had encountered serious financial problems in the early 1980s and, in November 1988, after an extended financial struggle, was sold to Robert Maxwell, a British tabloid tycoon. Allegedly Maxwell paid $2.6 billion for that prestigious New York publishing house, Macmillan, even though not a penny of the price came from his own fortune. It was all borrowed money (Thomas and Dillon, 2002).

One of the first of Maxwell’s publishing decisions was to close the Macmillan College Division, and the book, among other volumes in the series, landed in secondhand bookstores. College textbooks were of no particular interest to Maxwell. And before long Robert Maxwell drowned mysteriously: He allegedly fell off his yacht while sailing alone. Soon it became known that he had also been drowning in financial problems at the time.

The impact of this drama was to thrust the book out of print.

For several years and with chagrin I accepted as fact that my primate book had been terminated, and other interests took over. After a time, however, I began to receive urgent and increasingly frequent requests from colleges and universities to give permission for duplication of the book. Many colleagues and students voiced their hope that I would rewrite and publish a second edition.

In 1994, with the never-tiring encouragement of my husband, Elwyn L. Simons, and friends and colleagues, I decided to find out whether any publisher would be interested in publishing a new, totally rewritten and expanded version of the 1983 primate book. Thanks to the efforts and assistance of Dr. Charles Crumly and the inspiring reassurance and support of my dear friend Tab Rasmussen, I was able to sign a contract with Academic Press.

The process of rewriting the book began. My only good excuse for any delay was the fact that this book has been entirely a one-woman endeavor: Text, ideas, almost all illustrations, as well as the typing have been produced by me alone. Any author could spend an entire lifetime writing a textbook about our intriguing and fascinating relatives, the primates. There is constantly something new, exciting, and different that could be included. But every author must find the right moment when it is time to say it is done. This time has now arrived for the third edition.

I hope that all those who teach primatology with the help of this book will achieve teacher-student relationships of mutual respect, that is, of the love for teaching and learning together. Teaching and learning, even though not always easy, should be a mutually rewarding and inspiring adventure. I have all too often encountered university, college, and high school teachers whose uncaring arrogance hurt and permanently destroyed their outstanding students’ interest and inquisitiveness.

Though I do claim this book for my very own production and as I am taking responsibility for all of it, many others helped the project forward. My family, many friends, and many colleagues, including many of my students, all in some way or another aided and supported this work. Much of the initial impetus came from my students in Switzerland, in Germany, at Yale and Brown Universities, as well as at Duke University. My students have inspired me in much of what I have to say today. I cannot possibly name them all.

A large group of living primates, human and non-human alike, have obliviously provided me with insights and many opportunities to learn. These individuals have taught me most of what I know. Among much else they have shown me that their lives are above and beyond much of what is written about them in scientific publications. I often feel (and have also told my students) how it is a shame that non-human primates are unable to read all the papers and books written about them. Were they able to read about the things that they are supposed to be doing, they would well understand how they all too often do not conform to the tales that are written about their way of life. Perhaps they would feel indignant. I hope that I have not betrayed their anonymous trust and that I have portrayed them properly.

We humans must now fear for the primates’ chances to survive the unstoppable, all-consuming tidal wave of human population increase. As the one abundant species of primates rapidly overcrowds, mindlessly exploits, and overwhelms our planet, the non-human primates and many other living things are vanishing rapidly.

As things stand now there are too many of us humans, and we are destroying our closest relatives rapidly, just as we crowd out their habitats. We humans appear to be helpless, unable to deal with this cataclysmic dilemma. Even though we believe that we ourselves are the superior beings on Earth, we are proving to be ultimately destructive, unable to learn from experience, unable to properly plan for the future, and totally lacking respect for Mother Nature’s creations. It makes me wonder whether humans ever will be able to live up to their taxonomic name: Homo sapiens. The Latin word sapiens means wise, but are we wise enough to prevent our own destruction?

No matter what the future of humankind may be, I offer my deeply felt gratitude to many humans, friends, and colleagues alike.

Foremost, I would like to thank my family, Elwyn, Cornelia, Erik, and Verne, for their never-ending support, encouragement, patience, help, understanding, and love. Tab Rasmussen, Patricia C. Wright, and Terry Maltsberger should be singled out, for they have been more than understanding friends. Tab is a most inspired and inspiring force behind many fruitful professional discussions; he has provided incentive, advice, constructive criticism, and ideas all along. Terry Maltsberger has scampered untiringly around zoos, helping to obtain good photographs of primates for this book. Like Elwyn, Terry has been immensely helpful with encouragement and straightening out the sometimes confounding intricacies of the English language, which, after all, is only my second language. (I am getting better at this.)

At times it can be truly vexing to write in a language one did not speak while growing up. Our son Verne told me about the Danish comedian Victor Borge, who concisely expressed it by stating: English is not my language. I am just trying to use it.

The number of those who have assisted me in various ways is increasing. I would like to mention by name John M. Allman, David Anderson, Summer Arrigo-Nelson, Edilio Nacimento Becerra, Diane Brockman, Anne Burroughs, Jennifer Campbell, Anita Christen, Anja Deppe, Luke Dollar, John Fleagle, Jörg Ganshorn, Phil Gingerich, Ken Glander, Laurie Godfrey, David Haring, Mitchell Irvin, Karen Issler, Jukka Jernvall, Chris Kirk, Jeffrey Laitman, Coleen McCann, Russel Nord, Theresa Pope, Leila Porter, Tab Rasmussen, Marcello Rosa, James Rossie, Marcello Sánchez-Villagra, Erik Seiffert, Verne Simons, Timothy Smith, Tom Struhsaker, Michael Stuart, Linda Taylor, Donald Usery, and Priscilla Watson for their generous help with hard-to-find literature, information, or photographs. Carol Holman kindly donated the elusive volume about the Creatures of the Dark. Tristram Wyatt also helped with insight and advice, and each has contributed in special ways and deserves my special gratitude. John Fleagle wrote the thoughtful foreword to the second edition.

Kathleen Caron did a terrific job straightening out details of molecular and cell biology. Dieter Glaser thoroughly inspected and improved the chapters on olfaction and taste. Ralph Holloway critiqued and checked the chapter on the brain for correctness. For the second edition, Charles Crumly proffered a challenge that I happily lived up to: namely to include a chapter on molecular primatology.

Jukka Jernvall suggested that the third edition must have a chapter on primate genomics, a very complex issue that I hope to have dealt with successfully. Special thanks go to Patrick O’Connor—who took on the tiring task of reading and improving the vision chapter. James Pettigrew also provided important insights and information about vision. Timothy Smith spent much time discussing olfaction and the vomeronasal organ with me and did not hesitate to share published and as yet unpublished data and figures. Patricia C. Wright played a particularly important role during the process of putting this volume together—she generously contributed her knowledge, improving the new chapters about the primate senses. Pat also provided much new data and knowledge about Madagascar and New World primates and always is ready with much thought and much appreciated encouragement.

Just when I thought I had finished the task, suddenly and out of the blue, Richard Tenaza refreshed long-forgotten memories about the fact that primates have a third, nictitating membrane. Thank you, Richard Tenaza, for this important message that prompted me to go back and write yet another paragraph.

Finally, I would particularly like to express my gratitude to the editorial staff of Elsevier. To David Cella and Nancy Maragioglio, who approached me about the possibility of preparing a third edition of Primate Anatomy: An Introduction. To Kelly Sonnack, who authenticated my contract. To Tamsin Leonard, who met with me in Oxford; to Sarah Hajduk and Rogue Shindler, who both provided valuable editorial assistance; and last but not least, especially to Julie Louis from Graphic World, who never tired to provide excellent editorial advice and to take care of last-minute changes and brainstorms. My heartfelt thanks go to you all for your help, patience, excellent advice, and support: I could not have done it without you.

And finally here is the much improved third edition. Preparing this new edition I have learned uncountable new facts, and I hope that this is now reflected in the third edition of Primate Anatomy: An Introduction.

As all authors endeavor to profess, all and every mistake in this book should be blamed on me and me alone. This is my book, I am proud of it, and I will gladly take responsibility for it all.

Friderun Ankel-Simons,     Durham, September 2006

Preface to the First Edition

Many people give various kinds of help to an author during the preparation of a book. Such aid—both explicit and implicit—deserves the author’s thanks.

First, I thank my students, whose inquisitive questions have always been an invaluable stimulus that has taught me more than many teachers have.

Furthermore, my gratitude goes to all those colleagues who assisted me in various ways and especially to those who read and contributed their criticism to parts of the book, namely Fredericka Oakley, Matt Cartmill, Bert Covert, Dieter Glaser, Andy Hamilton, David Pilbeam, Montrose Moses, Patricia Poorman, Len Radinsky, and Ian Tattersall. Rich Kay also helped with some library problems. My husband, Elwyn Simons, edited the manuscript and added much invaluable knowledge and advice. Ruth Nix was helpful with editorial matters.

I am also very grateful to all those who contributed photographs: Alison Richard, Ken Glander, Dieter Glaser, Christian Schmidt, Michael Stuart, and Heinrich Sprankel.

Last, my dear friend Elsa Dubois gave me support in so many ways that a very special word of thanks goes to her.

One final word about the scope of this book seems appropriate here. Because both the primate fossil record and the details of behavior of living primates have already been covered by Elwyn Simons and Alison Jolly in their respective contributions to the Macmillan Series in Physical Anthropology, no attempt is made here to duplicate any of the information included in their two volumes.

F.A.S.,     New Haven, 1983

Chapter 1

Taxonomic List of Extant Primates

Publisher Summary

This chapter provides an introduction to primate that is one of the most diversified groups of living mammals, ranging from lemurs to humans. Members of the order have always been the focus of human curiosity, and many primates are astonishingly similar, both behaviorally and anatomically, to human beings, the most successful and progressive species of the order is Homo sapiens. The chapter provides a list of taxonomic names to become familiar with the wide variety and diversity of primates. This list is the foundation and necessary frame of reference for informed discussion about primates. The particular taxonomic place and common name of each species is helpful in increasing knowledge of primates and their characteristics.

New Developments

List of Extant Primates

NEW DEVELOPMENTS

The order Primates is one of the most diversified groups of living mammals, ranging from lemurs to humans. Members of the order have always been the focus of human curiosity, and many primates are astonishingly similar, both behaviorally and anatomically, to human beings, the most successful and progressive species of the order: Homo sapiens.

To become familiar with the wide variety and diversity of primates, it is helpful to look over the following list of taxonomic names. The rationale of beginning this book with a comprehensive list of all living primates is that an introduction to the particular taxonomic place and common name of each species will enable the reader to understand more readily the subsequent chapters. Naturally, it takes patience to become familiar with all of the primate groups, and this knowledge will only improve gradually and with time. One should become acquainted, but there is no need to memorize the list of names. These names will fall into place with increased knowledge of and interest in the primates and their characteristics.

It must be kept in mind, however, that taxonomic assignments are subject to constant change, new discovery, and discussion. The following list is the foundation and necessary frame of reference for informed discussion about primates. New discoveries can either change a taxonomic placement of known animals through new insights or add newly discovered species that were hitherto unknown to science. The astonishing increase of species in many genera can be credited to two factors: the increase of the number of primatologists in the field worldwide who find hitherto unknown taxa and the proliferation of new assignments by primatologists who stay home and increase and change the number of species by desktop contemplations. The recent proliferation of many new species from Madagascar is nothing short of astonishing, although all too often these discoveries appear to be based more on the enthusiasm of the discoverers than on unambiguous morphological, genetic, and behavioral distinctions. Surprisingly however, even among living primates, true new species are still occasionally being described. For example, a new species of macaque from northern India, Macaca munzala, was described in 2005 (Sinha et al.). A new species from Tanzania was described as Lophocebus kipunji in 2005 (Jones et al.), but was reassigned to a new genus, Rungwecebus, by Davenport et al. (2006). This shows that some species are truly new, whereas others may either be valid or produced by excessive redefinitions, rearrangements, new rankings, and splits of formerly known taxa.

Patricia Wright and Elwyn Simons have been working in Madagascar since 1981, actively promoting conservation of the rare and endangered lemurs for the future. Both were crucially involved in opening up the magic island for international research and were soon followed by myriad others. Because of this, there can be no doubt that our knowledge about Malagasy lemurs in particular and Madagascar’s natural history in general have vastly increased since that time.

The following lineup of living primates is based on the taxonomy of Simons (1972), which has been brought up to the knowledge of 1999 with the help of Patricia Wright and Elwyn Simons for prosimians, Thomas Struhsaker for colobines, and Leslie Digby for callithrichids. The list has been amended for this edition using the texts by Groves (2001) and Geissmann (2003) for all primates, Grubb et al. (2003) for African primates, Brandon-Jones et al. (2004) for Asian primates, and Wright et al. (2003) for genus Tarsius. Unlike Grubb et al. (2003), we are not dealing with subspecies in our lineup of living primates. The taxonomy and phylogeny of the subtribe Papionina has long been under discussion (Jolly, 2003). It appears that now the puzzle surrounding the baboons has been solved to some extent by a very interesting and thorough evaluation of cranial allometry, phylogeny, geographic distribution, and systematics of the papionins. The information has been evaluated with the help of geometric morphometric analysis landmark data and resulted in the confirmation of three genera: Mandrillus with two species, Theropithecus with one species, and Papio with one species, P. hamadryas, that has six subspecies (Frost et al., 2003). We are not listing subspecies because the taxonomic list of all primates would be too long and cumbersome for this chapter. Also the postcranial morphology and dentition of the papionins has been evaluated to reassess molecular evidence that had separated terrestrial mangabeys (genus Cercocebus) together with genus Mandrillus from the arboreal mangabeys (genus Lophocebus) together with genus Papio. Fleagle and McGraw (2002) have established that postcranial and dental characters support a previous molecular assignment.

Additional sources for the following lineup have been Mittermeier et al. (1994) for lemurs, Rowe (1996) for all primates, Gautier-Hion et al. (1988) for the African guenons (genus Cercopithecus), Davies and Oates (1994) for colobine monkeys, and Baer et al. (1994) for new taxonomic insights concerning the South American owl monkey Aotus.

The book dealing with all extant primates (Rowe, 1996) provides detailed information about each species and is illustrated by excellent photographs. These various resources have all helped to complete the following taxonomic lineup of living primates. Their geographic distribution is shown in Figure 1.1.

Figure 1.1 Worldwide distribution of primates: not unlike body weight data, animal distribution maps are subject to constant change resulting from human impact, newly confirmed sightings, and other unpredictable factors.

Many subspecies of Malagasy lemurs and other primates have been elevated to species level (Rasolooarison et al., 2000; Groves, 2001; Brandon-Jones 2004; Thalmann and Geissmann, 2000, 2005). The new species are included in the lineup, although the justification for such changes in taxonomic ranking remains under discussion. New and formerly unfamiliar names are used in publications and therefore they are listed here.

LIST OF EXTANT PRIMATES

Suborder Prosimii (Illiger, 1811)

Infraorder Lemuriformes (Gregory, 1915)

Superfamily Lemuroidea (Mivart, 1864)

Family Cheirogaleidae (Gray, 1873)

Subfamily Cheirogaleinae (Gray, 1873)

¹

²

³

⁴

⁵

⁶

⁷

⁸

⁹

¹⁰

¹¹

¹²

¹³

¹⁴

¹⁵

¹⁶

¹⁷

¹⁸

¹⁹

²⁰

¹New species described by Kappeler et al., 2005.

²Rumpler (1975) separates from Lemuridae the genus Lepilemur as a fifth family, Lepilemuridae. Lepilemur is now listed by some in the family of subfossil Megaladapis with two subfamilies: the subfossils in Megaladapinae and the living species in Lepilemurinae (Mittermeier et al., 1994; Shoshani et al., 1996). *Several new species have been announced, their description has not yet been published.

³Eulemur: new generic name for species of Lemur other than Lemur catta. C.R. Acad. Science Paris, Ser. 3, 307:547–551. (Not Petterus because Groves and Eaglen 1988 was published after Simons and Rumpler, 1988).

⁴A new Avahi species was recently named, A. cleesei (Thalmann and Geissmann, 2005) that has been based solely on geography, fur coloration, and video and audiotape data.

⁵In 1987, P. Jenkins pointed out that the family name Lorisidae was preceded in time by Loridae (Gray, 1921). However, J.H. Schwartz et al. (1998) submitted an appeal to suppress Loridae in favor of Lorisidae. Lorisidae has been reinstated and is used in this text.

⁶Regarded to be a subspecies of N. coucang by Brandon-Jones et al. (2004).

⁷In 1996, J.H. Schwartz described a new genus and species "Pseudopotto based on a virtually complete skeleton and adult dentition and one partial skull, mandible and mixed dentition" skeletal museum specimens. The names of genera Galagoides, Otolemur, and Euoticus are listed in parenthesis although they have been declared invalid and unwarranted (Nash et al., 1989). I follow this suggestion and use the genus designation Galago for all bushbabies.

⁸Genus Aotus was subdivided by Hershkovitz in 1983 into two species groups with a total of nine species. A careful study of taxonomy and distribution of genus Aotus by S.M. Ford in 1994 reduced the number of species to between five to seven, which are recorded here.

⁹In 2002, a Taxonomic review of the Titi monkeys, Genus Callicebus, was published (van Roosmalen et al., 2002).

¹⁰Hershkovitz (1979, 1987) established five species of genus Pithecia.

¹¹There are two species of Chiropotes according to Hershkovitz (1985).

¹²Defler and Hernández-Camacho (2002) discussed C. albifrons albifrons subspecies assignments.

¹³Surprisingly, Callitrichidae and Callitrichinae are also often spelled Callithrichidae and Callithrichinae.

¹⁴Regarded to be genus Oedipomidas by some.

¹⁵Several species of Cercopithecus have been assigned to the super genus Chlorocebus (Vervets), and the genus is in need of revision (Groves, 2001). I continue to use genus Cercopithecus here.

¹⁶A new species of Lophocebus, L. kipunji (Jones et al., 2005) made news in 2005, but has since been reassigned to its own genus: Rungwecebus kipunji (Davenport et al., 2006).

¹⁷The following species are regarded as subspecies of Colobus (Piliocolobus) badius by some authors.

¹⁸Genus Hylobates has been subdivided into genera Bunopithecus, Hylobates, and Nomascus (Geissmann, 2003; Brandon-Jones et al., 2004).

¹⁹Genus Symphalangus is now regarded to be a subgenus of Hylobates by some.

²⁰An alternative taxonomy puts Pongidae into superfamily Pongoidea and our own family, Hominidae, into superfamily Hominoidea.

Chapter 2

Taxonomy

Publisher Summary

This chapter provides a brief overview of classification of animals and plants. The essence of classification is to order all living things into groups that not only resemble each other but are also related to each other by evolution through time. This ordering allows scientists in all fields to communicate effectively with one another about the natural world in which we all live. The classification methodology should be stable to support widespread understanding. In a commonly used classification system, all known living organisms are grouped into five kingdoms—Monera, Protista, Fungi, Plantae, and Animalia. These kingdoms are ordered into smaller categories, namely, into phyla, classes, orders, families, genera, and species. Species that are defined according to similarity are called morphological species. At present, three discrete methodologies of classification are recognized—traditional or evolutionary classification—this kind of classification begins with the assessment of overall morphological similarity between organisms. Similarities are tested for patterns of homologies in living organisms and, if possible, are compared with fossil forms; numerical or phenetic taxonomy—numerical taxonomy essentially depends on equal weighting of all phenetic characters and it totally rejects phylogenetic implications because phylogenetic events are considered to be scientifically unverifiable; and cladistics—the taxonomic method of cladistics is based on the claim for objectivity as numerical phenetic classification.

Hierarchical Classification

Population Biology and Classification

Traditional (or Evolutionary) Classification

Numerical (or Phenetic) Taxonomy

Cladistics

Misunderstandings in Primate Classification

The Tarsier Conundrum

Human minds are constantly trying to rank or sort out all that surrounds them. Animate as well as inanimate objects are always consciously or unconsciously classified. Humans among themselves are also constantly judged and sorted—within and between groups—and consequently we could say that appraising others and the world around us is part of the human condition. Thus, it appears that human beings have classifying minds. Classification involves all aspects of daily life, even though it is disguised by different names: decision making, selection, planning, pigeonholing, discriminating, and judging are some of the terms that describe classifying endeavors.

Looking back into our past, it appears that classification may have already begun when humans first started to reason. During early human history, and even in prehistoric times, we can find rock and cave art that document how human beings perceive themselves in comparison to animals.

One of the first works to have put classification of the animal world in print is Aristotle’s Historia Animalium (384–322 b.c.). This early written attempt of animal classification appears to be based on real insight and knowledge concerning the animated world (Mayr, 1982). In fact, Aristotle was the first great natural historian, and his history of the animals was only the beginning of more or less elaborate attempts by early scientists to classify both animals and plants scientifically. These initial efforts to classify nature were purely comparative and based on morphology. Numerous natural history collections were established in Europe during the late fourteenth century when explorers traveled farther than ever before and returned with strange plants and animals, including shells, dried plants, feathers, skeletons, and skins quite unlike those to be found in their native lands.

The fascination with nature prevalent at this time led to a rapid increase in knowledge about the biotic diversity of the world around us. Attempts to classify nature finally culminated in the Systema Naturae (1758, 10th edition) by the Swedish botanist Carolus Linnaeus (1707–78). He created the system of binomial nomenclature for all animals and plants using Latin names for genus and species. His basic binomial methodology of genus and species assignment still prevails.

The goal of science is to find evidence for observable facts—any test of validity must be repeatable. However, this evidence is subject to constant revision as knowledge grows. In biology, we must be content with the immutable certainty that phenomena and evolutionary conclusions cannot be as indisputable as physical or mathematical proofs. Biology is innately unorganized and inherently variable. This does not mean, however, that biological rules can be doubted. The notions of intelligent design and creation clearly reside beyond scientific knowledge and simply belong in the realm of naive and undisputed faith.

The all-encompassing realm of animal life is Linnaeus’s highest category: the kingdom Animalia. Within the kingdom, all animals with axial skeletons are categorized in phylum Chordata. The next entity is the class Mammalia, including all mammals. Within mammals, a further step down is the order Primates, including prosimians, tarsiers, monkeys, apes, and humans. All primates are then grouped into families, each of which contains closely related genera and, finally, species. In this system, the genus name (equivalent to the family name) is a Latin (or latinized Greek) name in the nominative singular. The genus name determines a group of similar organisms. The genus then is further divided into species. Species are groups of animals or plants that are able to reproduce sexually with each other and produce fully fertile offspring. Species are assigned the second name that is not capitalized and is usually an adjective that agrees grammatically with the genus name (e.g., Homo sapiens, where Homo is the Latin name for humans and sapiens means intelligent; Pan troglodytes for the chimpanzee, where Pan is the Latin name for the mythical God of the forest and troglodytes is Greek for cave dweller). Both genus (plural of genus = genera) and species (plural = species) names are usually printed in italics (or underlined). For example, the name for the common chimpanzee is genus Pan and species troglodytes = Pan troglodytes; the binomial name for the common macaque is Macaca mulatta. Linnaeus’s system is still in use today, almost 240 years after it was created. Linnaeus’s system used morphological characteristics for his classification and assumed that species and genera were unchangeable. Thus, his system was purely a typological classification lacking any other implications such as questions about relatedness. If a species is named for a person, the annotation should end with i, as, for example, Propithecus tattersalli, a species of lemur that was named as recently as 1988 (Simons, 1988).

It was Charles Darwin who not only recognized but also published the important insight that the abundance of living forms has evolved throughout time in his Origin of Species. In the introduction to the third edition (1861, p. 3), Darwin stated:

In considering the Origin of Species, it is quite conceivable that a naturalist, reflecting on the mutual affinities of organic beings, on their embryological relations, their geographical distribution, geological succession, and other such facts, might come to the conclusion that each species had not been independently created, but had descended, like varieties, from other species.

Darwin pointed out how variability is of crucial importance for the modification of species throughout long periods of time. He concluded, based on his observations, that all living organisms must be descended from a common ancestor and that all living things are connected to each other through time by genealogical relationships. Thus, it was Darwin who first made it clear that all classification of living organisms is hierarchical and therefore should be genealogical.

HIERARCHICAL CLASSIFICATION

Ultimately the essence of classification is to order all living things into groups that not only resemble each other but are also related to each other by evolution through time. This ordering allows scientists in all fields to communicate effectively with one another about the natural world in which we all live. Classification methodology should be stable to support widespread understanding and not confusion.

Linnaeus only recognized the kingdoms of Animalia and Plantae. In a now commonly used system, all known living organisms are grouped into five kingdoms: Monera, Protista, Fungi, Plantae, and Animalia. These kingdoms are ordered into smaller categories (in descending order), namely, into phyla (singular = phylum), classes, orders, families, genera, and species. Species that are defined according to similarity are called morphological species.

For example, the place of one primate species in the realm of classification within the animal kingdom is as follows:

The chimpanzee Pan troglodytes is classified in the

Classification of all organisms is structured in such a hierarchical way, putting groups of similar organisms within higher groups of less similar organisms and so on. All of these categories just described have also been subdivided into various further, more detailed groups with the help of the prefixes sub- or super-!.

During the 100 years following Linnaeus’s initial classification and the publication of Darwin’s theory of evolution, there was much written and philosophized about the astonishing wealth of plants and animals on Earth. Early on, humans were able to grasp the fact that there seems to be a gradient of morphological and organismal complication within the plant and animal kingdoms. Many attempts were made to explain this fact. Only during the end of the nineteenth and the first half of the twentieth centuries did it become increasingly clear that today’s biological complexity is the result of change through time (evolutionary change). This understanding led to the conclusion that classification should also incorporate information about evolutionary descent. Thus, systematics took on the added dimension of evolutionary systematics or phylogeny.

POPULATION BIOLOGY AND CLASSIFICATION

In the first half of the twentieth century, scientists began to understand that the species definition had to be formalized to include dynamic biological facts about relatedness. The term species took on the interpretation of population or a group of organisms of the same kind. In 1963, Ernst Mayr defined the term species functionally as a reproductive unit and thus profoundly changed the insight of biologists in regard to the true meaning of taxonomy (see also Groves, 2001, pp. 26–27). Ernst Mayr’s definition of the biological species is as follows: A species is a group of interbreeding natural populations that is reproductively isolated from other such groups.

There are many other species concepts, such as the morphological or typological species concept that pertains to fossils but cannot be easily defined because of the factor of time that is involved in the definition of a fossil species. Today the taxonomic grouping of organisms is supported by morphological, structural, behavioral, and biochemical similarity. Similarities between organisms that are based solely on their life in the same environment—such as the shape of fish and sea mammals or birds and bats—are not decisive classificatory factors. Fish and dolphins are not very closely related, nor are birds and bats. Even though the lifestyle and basic shape of fish and dolphins are similar, their ancestors were very different. These two forms live in the same aquatic environment, but their superficial similarity of appearance is homoplastic (or analogous)—caused by living in the same substrate and not by a close evolutionary relationship. On the other hand, the skeletons of the forelimbs of bats and of primates are made up of the same bones and are homologous to each other. Although functionally vastly different, their forelimb bones are similar because of common ancestry. Homology is one of the significant criteria on which classification ideally should be based.

Today classification is a field so vast that it is not possible here even to scratch the surface of all the publications that concern it or even to mention all the books and articles that have dealt with it. Classification, in one sense, has also caused much difficulty, because it unfortunately and inevitably leads some to discrimination, and ultimately racism. Classification in the field of biology is no less controversial than it is in everyday life.

There can be no doubt that ever since Darwin’s time, all evolutionary biologists have recognized the crucial importance of phylogeny—the evolutionary history or line of an organism’s descent—in classification. Even those biologists who have rejected phylogeny as the basis for classification, such as pheneticists and to a degree also cladists, did so because they decided that phylogeny was impossible to know with certainty and was therefore useless. One of the key problems of classification is that geological lines of descent can only be factual to a certain degree, and therefore other equally logical classifications of groups of organisms in a phylogeny are often proposed.

At present, we recognize three discrete methodologies of classification: traditional (or evolutionary) classification, numerical (or phenetic) taxonomy, and cladistics. (For in-depth discussions, see Cartmill, 1981; Mayr, 1982; Mayr and Ashlock, 1991; Groves, 2001.)

TRADITIONAL (OR EVOLUTIONARY) CLASSIFICATION

This kind of classification begins with the assessment of overall morphological similarity between organisms. Similarities are tested for patterns of homologies in living organisms and, if possible, are compared with fossil forms. Criteria concerning ontogenetic development, cell biology or biochemistry, physiology, and behavior can also be of importance. As many factors as possible should go into such a classification. Similarities within groups of organisms that are classified together—for example, prosimians or insectivores—are also evaluated in regard to their phylogenetic or evolutionary relationship when attempts are made to link them with each other. Such relationships among organisms are often portrayed with the help of phylogenetic trees. Phylogenetic trees visually illustrate ancestor–descendant relationships as well as the passage of time involved in the evolution of taxa (a taxon [plural = taxa] being a natural unit of organisms that are grouped together and given a common name because they do have a number of characteristics in common). It must be stressed that phylogenetic trees do not represent classification, because phylogenetic trees are striving to present visually purported lines of descent. In contrast, classification only attempts to group organisms according to characteristics they have in common. Knowledge about, and considerable experience with, a particular group of organisms is an essential prerequisite for any construction of a valid classification because of the great complexity of factors that come into play. An ideal system also includes information about the evolutionary relationship between the classified organisms. This kind of traditional or evolutionary classification has been criticized because it relies on individual experience and observation by researchers and can thus be biased.

In the 1940s and 1950s, biologists increasingly began to realize the need for better and more exacting methods of classification. Specifically, classificatory methods that might be considered unbiased, repeatable, and indisputably correct were sought. This endeavor led to the proposal of two new methodologies: numerical (or phenetic) taxonomy and cladistics.

NUMERICAL (OR PHENETIC) TAXONOMY

Developed and refined during the first half of the twentieth century, numerical taxonomy essentially depends on equal weighting of all phenetic (that is, visible; Greek pheno = making visible, to show) characters (as many as possible) and it totally rejects phylogenetic implications because phylogenetic events are considered to be scientifically unverifiable (Sneath and Sokal, 1976; Sokal, 1974). This means that all characters evaluated are of equal importance. This method claims to be strictly objective. Numerical or phenetic taxonomy is not new, but has been accelerated in its development by the rapidly increasing availability of refined computer technology as well as the availability of biochemical sequence data of living organisms. Computer programs that cluster taxa together based on quantitative measures of overall similarity can quickly produce multiple variants of assumed relationships that are based on numerical character data. These methods claim to be simple and repeatable. They do not require any previous knowledge of a taxon that is classified. Numerical phenetics has not been used much in primatology recently except in applications for DNA sequence data. The cluster methods used have traditionally been modified to link taxa because of certain nucleotides they share. (For detailed discussions, see Mayr and Ashlock, 1991.)

Cladistics

During the last years of World War II, a young scientist, Willi Hennig, in war-torn Germany struggled with classification problems involving the insects with which he was working. His struggle was intense because he was somewhat isolated. Most of his peers and teachers were gone, involved in the war and unavailable for helpful discussions. His endeavors cumulated in the 1950 publication of a book in which he presented his theoretical ideas and a new terminology of phylogenetic systematics. In 1966, a variation, not an exact translation, of Hennig’s original book and ideas about phylogenetic systematics was published in the United States, where his method of classification soon became fashionable. Hennegian classification techniques and Hennig’s new and cumbersome terminology are taught everywhere. The taxonomic method of cladistics is based on the same overall claim for objectivity as numerical phenetic classification. What makes the cladistic method different is the assumption that phylogeny occurs only by means of dichotomies: a parent taxon splits into two sister taxa, and the parent taxon ceases to exist after the split—an assumption that some have called absurd (Cartmill, 1981). The determination of a dichotomy should, according to Hennig, be based solely on the common possession of uniquely derived characters (called synapomorphies by Hennig). Such classifications are only workable for the evaluation of few characters at a time; otherwise, they become overwhelmingly complex.

All classification schemes have to be based on the different information value contained in morphological, behavioral, or molecular characters. Characters are the basis for any and every biological taxonomy and have to be chosen by the researcher. Cladistic systematics requires overly simplified recording of characters. Most variable morphological features are reduced to two or more so-called character states. These character states are coded as 0, 1, or 2, although multistate characters are sometimes allowed. Thus, cladistic systematics is a labor-intensive recording of numerous characters, which—especially where fossils are concerned—are often numerical measurements. These characters have to be appraised as to their systematic value and are weighted according to their intrinsic meaning for subsequent systematic evaluation. Weighting of characters is also practiced in traditional taxonomy because characters defining organisms are not all of equal value. The evaluation of as many characters as possible results in long lists of weighted characters and computer-generated treelike diagrams. All cladistic trees are essentially digital,¹ with a parental taxonomic unit splitting into two offspring taxa (also called sister or sibling groups). Even